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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Phloem: the integrative avenue for resource distribution, signaling, and defense</title>
<author><name sortKey="Van Bel, Aart J E" sort="Van Bel, Aart J E" uniqKey="Van Bel A" first="Aart J. E." last="Van Bel">Aart J. E. Van Bel</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Biology, Institute of General Botany, Justus-Liebig-University</institution>
<country>Giessen, Germany</country>
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<author><name sortKey="Helariutta, Yk" sort="Helariutta, Yk" uniqKey="Helariutta Y" first="Yk" last="Helariutta">Yk Helariutta</name>
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<country>Helsinki, Finland</country>
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<author><name sortKey="Thompson, Gary A" sort="Thompson, Gary A" uniqKey="Thompson G" first="Gary A." last="Thompson">Gary A. Thompson</name>
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<author><name sortKey="Ton, Jurriaan" sort="Ton, Jurriaan" uniqKey="Ton J" first="Jurriaan" last="Ton">Jurriaan Ton</name>
<affiliation><nlm:aff id="aff4"><institution>Department of Animal and Plant Sciences, University of Sheffield</institution>
<country>Sheffield, UK</country>
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<author><name sortKey="Dinant, Sylvie" sort="Dinant, Sylvie" uniqKey="Dinant S" first="Sylvie" last="Dinant">Sylvie Dinant</name>
<affiliation><nlm:aff id="aff5"><institution>Institut Jean-Pierre Bourgin UMR1318 INRA-AgroParisTech, Institut National de la Recherche Agronomique</institution>
<country>Versailles, France</country>
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</affiliation>
</author>
<author><name sortKey="Ding, Biao" sort="Ding, Biao" uniqKey="Ding B" first="Biao" last="Ding">Biao Ding</name>
<affiliation><nlm:aff id="aff6"><institution>Department of Molecular Genetics, The Ohio State University</institution>
<country>Columbus, OH, USA</country>
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</affiliation>
</author>
<author><name sortKey="Patrick, John W" sort="Patrick, John W" uniqKey="Patrick J" first="John W." last="Patrick">John W. Patrick</name>
<affiliation><nlm:aff id="aff7"><institution>School of Environmental and Life Sciences, The University of Newcastle</institution>
<country>Callaghan, NSW, Australia</country>
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<idno type="doi">10.3389/fpls.2013.00471</idno>
<date when="2013">2013</date>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Phloem: the integrative avenue for resource distribution, signaling, and defense</title>
<author><name sortKey="Van Bel, Aart J E" sort="Van Bel, Aart J E" uniqKey="Van Bel A" first="Aart J. E." last="Van Bel">Aart J. E. Van Bel</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Biology, Institute of General Botany, Justus-Liebig-University</institution>
<country>Giessen, Germany</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Helariutta, Yk" sort="Helariutta, Yk" uniqKey="Helariutta Y" first="Yk" last="Helariutta">Yk Helariutta</name>
<affiliation><nlm:aff id="aff2"><institution>Plant Molecular Biology Lab, Institute of Biotechnology, University of Helsinki</institution>
<country>Helsinki, Finland</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Thompson, Gary A" sort="Thompson, Gary A" uniqKey="Thompson G" first="Gary A." last="Thompson">Gary A. Thompson</name>
<affiliation><nlm:aff id="aff3"><institution>Department of Plant Science, College of Agricultural Sciences, The Pennsylvania State University, University Park</institution>
<country>PA, USA</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Ton, Jurriaan" sort="Ton, Jurriaan" uniqKey="Ton J" first="Jurriaan" last="Ton">Jurriaan Ton</name>
<affiliation><nlm:aff id="aff4"><institution>Department of Animal and Plant Sciences, University of Sheffield</institution>
<country>Sheffield, UK</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Dinant, Sylvie" sort="Dinant, Sylvie" uniqKey="Dinant S" first="Sylvie" last="Dinant">Sylvie Dinant</name>
<affiliation><nlm:aff id="aff5"><institution>Institut Jean-Pierre Bourgin UMR1318 INRA-AgroParisTech, Institut National de la Recherche Agronomique</institution>
<country>Versailles, France</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Ding, Biao" sort="Ding, Biao" uniqKey="Ding B" first="Biao" last="Ding">Biao Ding</name>
<affiliation><nlm:aff id="aff6"><institution>Department of Molecular Genetics, The Ohio State University</institution>
<country>Columbus, OH, USA</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Patrick, John W" sort="Patrick, John W" uniqKey="Patrick J" first="John W." last="Patrick">John W. Patrick</name>
<affiliation><nlm:aff id="aff7"><institution>School of Environmental and Life Sciences, The University of Newcastle</institution>
<country>Callaghan, NSW, Australia</country>
</nlm:aff>
</affiliation>
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<series><title level="j">Frontiers in Plant Science</title>
<idno type="eISSN">1664-462X</idno>
<imprint><date when="2013">2013</date>
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<pmc article-type="editorial"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Plant Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id>
<journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id>
<journal-title-group><journal-title>Frontiers in Plant Science</journal-title>
</journal-title-group>
<issn pub-type="epub">1664-462X</issn>
<publisher><publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">24324476</article-id>
<article-id pub-id-type="pmc">3838965</article-id>
<article-id pub-id-type="doi">10.3389/fpls.2013.00471</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Plant Science</subject>
<subj-group><subject>Editorial Article</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Phloem: the integrative avenue for resource distribution, signaling, and defense</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>van Bel</surname>
<given-names>Aart J. E.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001"><sup>*</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Helariutta</surname>
<given-names>Ykä</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Thompson</surname>
<given-names>Gary A.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ton</surname>
<given-names>Jurriaan</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dinant</surname>
<given-names>Sylvie</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ding</surname>
<given-names>Biao</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Patrick</surname>
<given-names>John W.</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>7</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup>
<institution>Department of Biology, Institute of General Botany, Justus-Liebig-University</institution>
<country>Giessen, Germany</country>
</aff>
<aff id="aff2"><sup>2</sup>
<institution>Plant Molecular Biology Lab, Institute of Biotechnology, University of Helsinki</institution>
<country>Helsinki, Finland</country>
</aff>
<aff id="aff3"><sup>3</sup>
<institution>Department of Plant Science, College of Agricultural Sciences, The Pennsylvania State University, University Park</institution>
<country>PA, USA</country>
</aff>
<aff id="aff4"><sup>4</sup>
<institution>Department of Animal and Plant Sciences, University of Sheffield</institution>
<country>Sheffield, UK</country>
</aff>
<aff id="aff5"><sup>5</sup>
<institution>Institut Jean-Pierre Bourgin UMR1318 INRA-AgroParisTech, Institut National de la Recherche Agronomique</institution>
<country>Versailles, France</country>
</aff>
<aff id="aff6"><sup>6</sup>
<institution>Department of Molecular Genetics, The Ohio State University</institution>
<country>Columbus, OH, USA</country>
</aff>
<aff id="aff7"><sup>7</sup>
<institution>School of Environmental and Life Sciences, The University of Newcastle</institution>
<country>Callaghan, NSW, Australia</country>
</aff>
<author-notes><corresp id="fn001">*Correspondence: <email xlink:type="simple">aart.v.bel@bot1.bio.uni-giessen.de</email>
</corresp>
<fn fn-type="other" id="fn002"><p>This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science.</p>
</fn>
<fn fn-type="edited-by"><p>Edited by: Steven C. Huber, Agricultural Research Service - US Department of Agriculture, USA</p>
</fn>
</author-notes>
<pub-date pub-type="epub"><day>25</day>
<month>11</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="collection"><year>2013</year>
</pub-date>
<volume>4</volume>
<elocation-id>471</elocation-id>
<history><date date-type="received"><day>25</day>
<month>10</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>31</day>
<month>10</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2013 van Bel, Helariutta, Thompson, Ton, Dinant, Ding and Patrick.</copyright-statement>
<copyright-year>2013</copyright-year>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/3.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p>
</license>
</permissions>
<kwd-group><kwd>phloem development</kwd>
<kwd>phloem physiology</kwd>
<kwd>phloem transport</kwd>
<kwd>phloem-located resistance</kwd>
<kwd>phloem-mobile signaling</kwd>
<kwd>phloem structure</kwd>
<kwd>phloem cell biology</kwd>
<kwd>electropotential waves</kwd>
</kwd-group>
<counts><fig-count count="0"></fig-count>
<table-count count="0"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="32"></ref-count>
<page-count count="3"></page-count>
<word-count count="2280"></word-count>
</counts>
</article-meta>
</front>
<body><p>Research over the past 20 years has revealed new functions of the phloem beyond resource allocation to a system that combines distribution and messaging (Thompson and van Bel, <xref ref-type="bibr" rid="B31">2013</xref>
) analogous to the circulatory and nervous systems in animals. Apart from allocating resources for maintenance and growth, the phloem distributes hormonal signals and a broad spectrum of protein- and RNA-based messages throughout the plant to regulate a myriad of physiological and developmental processes. Resources and signals, collectively, coordinate development, and growth as well as integrate responses to both biotic and abiotic environmental challenges. The transport of organic compounds such as sugars, amino acids, and lipidic substances through the phloem are exploited by a vast and diverse range of pathogens such as viruses, fungi, nematodes, aphids, and other phloem-feeding insects. Given its ubiquitous occurrence in land plants, the phloem seems to be the integrative tissue <italic>par excellence</italic>
. The contributions included in this research topic encompass the entire bandwidth of known phloem functions with emphasis on the diversity in structures and functions.</p>
<p>Differentiation and development of vascular cells is complex and not well understood. Vascular development partly depends on environmental cues that have also impacted the evolution of vascular systems and phloem transport mechanisms. A novel phylogenetic approach to identify genes involved in vascular development (Martinez-Navarro et al., <xref ref-type="bibr" rid="B26">2013</xref>
) shows that several vascular genes are expressed in green algae (Chlorophyta), the ancestors of land plants. Analysis of vascular genes in non-vascular and ancient vascular plants indicates that coordinated expression of gene sets led to the emergence of the present vascular system (Martinez-Navarro et al., <xref ref-type="bibr" rid="B26">2013</xref>
). Representatives of the Dof gene family are among the transcription factors involved in vascular differentiation (Le Hir and Bellini, <xref ref-type="bibr" rid="B22">2013</xref>
). Nematode saliva has the remarkable ability to induce re-differentiation of phloem cells and their neighbors with the objective to “tap” the sieve-tube sap (Absmanner et al., <xref ref-type="bibr" rid="B1">2013</xref>
).</p>
<p>Ample attention has been paid to the structural diversity, particularly in the phloem-loading zone, where environmental changes have unbuffered, and profound effects. The impact of diverse environmental conditions on leaf structure and carbohydrate processing is demonstrated with <italic>Arabidopsis</italic>
ecotypes (Adams et al., <xref ref-type="bibr" rid="B2">2013</xref>
; Cohu et al., <xref ref-type="bibr" rid="B9">2013a</xref>
,<xref ref-type="bibr" rid="B10">b</xref>
). Within the Asteridae, there is an immense diversity in minor-vein structures and companion cells (Batashev et al., <xref ref-type="bibr" rid="B4">2013</xref>
), which promises a higher variety of phloem-loading modes in dicots than previously suspected (Slewinski et al., <xref ref-type="bibr" rid="B29">2013</xref>
). It appears that a strict subdivision between apoplasmic and symplasmic phloem-loading species must be abandoned, since many species dispose over the devices to operate both modes in parallel. A structural feature of apoplasmic phloem loading in dicotyledons—the involvement of transfer cells—is highlighted in two contributions: one on the evolutionary trends, function and induction (Andriunas et al., <xref ref-type="bibr" rid="B3">2013</xref>
) and the other on transcriptional regulators of cell wall invagination (Chinnappa et al., <xref ref-type="bibr" rid="B8">2013</xref>
). A physiological feature of “active” symplasmic phloem loading is the size-selective transfer of sugars through plasmodesmata, which is challenged here using mathematical parameters (Liesche and Schulz, <xref ref-type="bibr" rid="B24">2013</xref>
). In grasses, the arrangement and ultrastructure of collection phloem suggest an apoplasmic mode of phloem loading (Botha, <xref ref-type="bibr" rid="B6">2013</xref>
; Slewinski et al., <xref ref-type="bibr" rid="B29">2013</xref>
). However, the functions of two principal structures in monocotyledonous leaves i.e., thick-walled sieve tubes and transverse veins remain puzzling (Botha, <xref ref-type="bibr" rid="B6">2013</xref>
). Thick-walled sieve tubes may be viewed as transformed phloem parenchyma cells (Slewinski et al., <xref ref-type="bibr" rid="B29">2013</xref>
) engaged in temporary storage (Botha, <xref ref-type="bibr" rid="B6">2013</xref>
).</p>
<p>Carbohydrate processing may be more homogeneous in transport phloem (Slewinski et al., <xref ref-type="bibr" rid="B29">2013</xref>
) than in the phloem-loading zone. Yet, permanently changing conditions require flexible and diverse solutions for release/retrieval along the pathway (De Schepper et al., <xref ref-type="bibr" rid="B11">2013</xref>
). Central to the release/retrieval concept is the intercellular competition for sugars that is revealed with electrical methods for <italic>in situ</italic>
measurement of sucrose uptake parameters (Hafke et al., <xref ref-type="bibr" rid="B15">2013</xref>
). The strong influence of environmental impacts on phloem functioning at each level is addressed in one comprehensive review by Lemoine et al. (<xref ref-type="bibr" rid="B23">2013</xref>
).</p>
<p>Long-distance signaling via the phloem can be accomplished by a variety of physiological mechanisms. Electrical signaling along sieve tubes affects both the physiology of distant leaves as well as photosynthate release/retrieval (Fromm et al., <xref ref-type="bibr" rid="B12">2013</xref>
). Long-distance effects of hormonal signaling on plant development have been demonstrated by expressing melon Aux/IAA genes into tomato plants (Golan et al., <xref ref-type="bibr" rid="B14">2013</xref>
). The translocation of microRNAs through the phloem regulates and coordinates distant processes such as mineral homeostasis (Kehr, <xref ref-type="bibr" rid="B20">2013</xref>
). Evidence is emerging for remote control of developmental processes in roots and tubers by phloem-mobile mRNAs (Hannapel et al., <xref ref-type="bibr" rid="B17">2013</xref>
). However, providing unambiguous evidence for some of the key processes implicated remains challenging and is open for debate (Hannapel, <xref ref-type="bibr" rid="B16">2013</xref>
; Suarez-Lopez, <xref ref-type="bibr" rid="B30">2013</xref>
).</p>
<p>RNA-species are most likely translocated as complexes with RNA-binding proteins (Pallas and Gomez, <xref ref-type="bibr" rid="B27">2013</xref>
). As RNAs, several viruses are translocated as ribonucleoprotein complexes (Hipper et al., <xref ref-type="bibr" rid="B18">2013</xref>
) which might protect the viral core against the adverse sieve-tube environment and/or confer tagging for invasion of specific target cells. While the viral complexes move through sieve tubes with the mass flow, phytoplasmas with sizes exceeding the diameters of the sieve pores—that are occluded anyway in response to infection—may be disseminated by alternative mechanisms. Remarkably, some plants species are able to overcome phytoplasma infection through the so-called “recovery reactions” that are mediated through callose degradation in sieve tubes (Santi et al., <xref ref-type="bibr" rid="B28">2013</xref>
).</p>
<p>The phloem contains attractants and repellents for animal pathogens. Present work indicates that sterols serve as attractants (Behmer et al., <xref ref-type="bibr" rid="B5">2013</xref>
) to phloem-feeding insects that have a deficient sterol synthesis, whereas benzylisoquinoline alkaloids serve as lethal repellents (Lee et al., <xref ref-type="bibr" rid="B21">2013</xref>
). It appears that phloem cells produce and transport an arsenal of defense compounds. The location of these anti-insect chemicals is significant e.g., for genetic manipulation of plants. Defense compounds against aphids may reside either or both in the pre-phloem pathway or inside the phloem cells themselves (Will et al., <xref ref-type="bibr" rid="B32">2013</xref>
). It is postulated that the major function of the extrafascicular phloem in cucurbits is to combat insects (Gaupels and Ghirardo, <xref ref-type="bibr" rid="B13">2013</xref>
). In legumes, giant proteins bodies (forisomes) may be involved in plant defense by rapid sieve-pore occlusion in response to an aphid attack (Jekat et al., <xref ref-type="bibr" rid="B19">2013</xref>
). The interactions between plants and aphids appear extremely complex (Louis and Shah, <xref ref-type="bibr" rid="B25">2013</xref>
) which hinders the development of molecular strategies for insect control. Nonetheless, strategies are being developed to increase the plant resistance against aphids (Will et al., <xref ref-type="bibr" rid="B32">2013</xref>
), and in one case by engineering of RFO phloem loading (Cao et al., <xref ref-type="bibr" rid="B7">2013</xref>
). The strong increment of RFOs in the sieve-tubes rendered the plants less attractive to aphids.</p>
<p>As with other research fields, phloem research reveals an ever receding horizon with undreamed possibilities. This topic shows the amazingly diverse ability of plants to cope with an infinite number of environmental challenges by virtue of the vascular tissues.</p>
</body>
<back><ack><p>We express our gratitude to all authors for their enthusiasm and dedication.</p>
</ack>
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